Coexistence of Borrelia burgdorferi s.l. genospecies within Ixodes ricinus ticks from central and eastern Poland
-
Hubert Sytykiewicz
,
Grzegorz Karbowiak
Abstract
The purpose of the study was to assess the prevalence and coinfection rates of Borrelia burgdorferi sensu lato genotypes in Ixodes ricinus (L.) ticks sampled from diverse localities in central and eastern regions of Poland. In years 2009-2011, questing nymphs and adults of I. ricinus were collected using a flagging method at 18 localities representing distinct ecosystem types: urban green areas, suburban forests and rural woodlands. Molecular detection of B. burgdorferi s.l. genospecies was based on amplification of a fla gene using nested PCR technique, subsequent PCR-RFLP analysis and bidirectional sequencing. It was revealed that 45 samples (2.1%) harboured two different B. burgdorferi s.l. genospecies, whereas triple infections with various spirochetes was found in 11 (0.5%) individuals. Generally, the highest average coinfection rates were evidenced in arachnids gathered at rural woodlands, intermediate at suburban forests, while the lowest were recorded at urban green areas. Overall, single spirochete infections were noted in 16.3% (n = 352/2,153) ticks. Importantly, it is the first report evidencing the occurrence of Borrelia miyamotoi (0.3%, n = 7/2153) in I. ricinus populations within central Poland. Circumstantial variability of B. burgdorferi s.l. genospecies in the common tick individuals sampled at various habitat types in central and eastern Poland was displayed. The coexistence of two or three different spirochete genospecies in single adult ticks, as well as the presence of B. miyamotoi were demonstrated. Therefore, further studies uncovering the co-circulation of the tested bacteria and other human pathogens in I. ricinus ticks are required.
References
Capelli G., Ravagnan S., Montarsi F., Ciocchetta S., Cazzin S., Porcellato E., Babiker A.M., Cassini R., Salviato A., Cattoli G., Otranto D. 2012. Occurrence and identification of risk areas of Ixodes ricinus-borne pathogens: a cost-effectiveness analysis in north-eastern Italy. Parasites & Vectors, 5, 61. DOI: 10.1186/1756-3305-5-6110.1186/1756-3305-5-61Search in Google Scholar PubMed PubMed Central
Cisak E., Chmielewska-Badora J., Zwoliński J., Wojcik-Fatla A., Zajac V., Skórska C., Dutkiewicz J. 2008. Study on Lyme borreliosis focus in the Lublin region (eastern Poland). Annals of Agricultural and Environmental Medicine, 15, 327-332Search in Google Scholar
Cisak E., Wójcik-Fatla A., Stojek N., Chmielewska-Badora J., Zwoliński J., Buczek A., Dutkiewicz J. 2006. Prevalence of Borrelia burgdorferi genospecies in Ixodes ricinus ticks from Lublin region (eastern Poland). Annals of Agricultural and Environmental Medicine, 13, 301-306Search in Google Scholar
Cosson J.F., Michelet L., Chotte J., Le Naour E., Cote M., Devillers E., Poulle M.L., Huet D., Galan M., Geller J., Moutailler S., Vayssier-Taussat M. 2014. Genetic characterization of the human relapsing fever spirochete Borrelia miyamotoi in vectors and animal reservoirs of Lyme disease spirochetes in France. Parasites & Vectors, 7, 233. DOI: 10.1186/1756-3305-7-23310.1186/1756-3305-7-233Search in Google Scholar PubMed PubMed Central
Derdáková M., Lencáková D. 2005. Association of genetic variability within the Borrelia burgdorferi sensu lato with the ecology, epidemiology of Lyme borreliosis in Europe. Annals of Agricultural and Environmental Medicine, 12, 165-172Search in Google Scholar
Dzięgiel B., Kubrak T., Adaszek Ł., Dębiak P., Wyłupek D., Bogucka-Kocka A., Lechowski J., Winiarczyk S. 2014. Prevalence of Babesia canis, Borrelia burgdorferi sensu lato, and Anaplasma phagocytophilum in hard ticks collected from meadows of Lubelskie Voivodship (eastern Poland). Bulletin of the Veterinary Institute in Pulawy, 58, 29-33. DOI: 10.2478/bvip-2014-000510.2478/bvip-2014-0005Search in Google Scholar
Ferquel E., Garnier M., Marie J., Bernède-Bauduin C., Baranton G., Pérez-Eid C., Postic D. 2006. Prevalence of Borrelia burgdorferi sensu lato and Anaplasmataceae members in Ixodes ricinus ticks in Alsace, a focus of Lyme borreliosis endemicity in France. Applied and Environmental Microbiology, 72, 3074-3078. DOI: 10.1128/AEM.72.4.3074-3078.200610.1128/AEM.72.4.3074-3078.2006Search in Google Scholar PubMed PubMed Central
Fingerle V., Schulte-Spechtel U.C., Ruzic-Sabljic E., Leonhard S., Hofmann H., Weber K., Pfister K., Strle F., Wilske B. 2008. Epidemiological aspects and molecular characterization of Borrelia burgdorferi s.l. from southern Germany with special respect to the new species Borrelia spielmanii sp. nov. International Journal of Medical Microbiology, 298, 279-29010.1016/j.ijmm.2007.05.002Search in Google Scholar PubMed
Geller J., Nazarova L., Katargina O., Golovljova I. 2013. Borrelia burgdorferi sensu lato prevalence in tick populations in Estonia. Parasites & Vectors, 6, 202. DOI: 10.1186/1756-3305-6-20210.1186/1756-3305-6-202Search in Google Scholar PubMed PubMed Central
Geller J., Nazarova L., Katargina O., Järvekülg L., Fomenko N., Golovljova I. 2012. Detection and genetic characterization of relapsing fever spirochete Borrelia miyamotoi in Estonian ticks. PLoS One, 7, e51914. DOI: 10.1371/journal.pone. 0051914Search in Google Scholar
Jenkins A., Hvidsten D., Matussek A., Lindgren P.E., Stuen S., Kristiansen B.E. 2012. Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from Norway: evaluation of a PCR test targeting the chromosomal flaB gene. Experimental and Applied Acarology, 58, 431-439. DOI: 10.1007/s10493-012-9585-210.1007/s10493-012-9585-2Search in Google Scholar PubMed PubMed Central
Lommano E., Bertaiola L., Dupasquier C., Gern L. 2012. Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in Western Switzerland. Applied and Environmental Microbiology, 78, 4606-4612. DOI: 10.1128/ AEM.07961-1110.1128/AEM.07961-11Search in Google Scholar PubMed PubMed Central
Pangrácová L., Derdáková M., Pekárik L., Hviščová I., Víchová B., Stanko M., Hlavatá H., Peťko B. 2013. Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasites & Vectors, 6, 238. DOI: 10.1186/1756-3305-6-23810.1186/1756-3305-6-238Search in Google Scholar PubMed PubMed Central
Pejchalová K., Zákovská A., Mejzlíková M., Halouzka J., Dendis M. 2007. Isolation, cultivation and identification of Borrelia burgdorferi genospecies from Ixodes ricinus ticks from the city of Brno, Czech Republic. Annals of Agricultural and Environmental Medicine, 14, 75-79Search in Google Scholar
Platonov A.E., Karan L.S., Kolyasnikova N.M., Makhneva N.A., Toporkova M.G., Maleev V.V., Fish D., Krause P.J. 2011. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerging Infectious Diseases, 17, 1816-1823. DOI: 10.3201/eid1710.10147410.3201/eid1710.101474Search in Google Scholar PubMed PubMed Central
Rosef O., Radzijevskaja J., Kløcker L., Paulauskas A. 2014. The prevalence of Borrelia burgdorferi sensu lato in questing Ixodes ricinus ticks in Norway. Biologija, 60, 33-45.Search in Google Scholar
Schulz M., Mahling M., Pfister K. 2014. Abundance and seasonal activity of questing Ixodes ricinus ticks in their natural habitats in southern Germany in 2011. Journal of Vector Ecology, 39, 56-65. DOI: 10.1111/j.1948-7134.2014.12070.x 10.1111/j.1948-7134.2014.12070.xSearch in Google Scholar
Schwarz A., Hönig V., Vavrušková Z., Grubhoffer L., Balczun C., Albring A., Schaub G.A. 2012. Abundance of Ixodes ricinus and prevalence of Borrelia burgdorferi s.l. in the nature reserve Siebengebirge, Germany, in comparison to three former studies from 1978 onwards. Parasites & Vectors, 5, 268. DOI: 10.1186/1756-3305-5-26810.1186/1756-3305-5-268Search in Google Scholar
Skotarczak B., Wodecka B., Cichocka A. 2002. Coexistence DNA of Borrelia burgdorferi sensu lato and Babesia microti in Ixodes ricinus ticks from north-western Poland. Annals of Agricultural and Environmental Medicine, 9, 25-28Search in Google Scholar
Smetanová K., Burri C., Pérez D., Gern L., Kocianová E. 2007. Detection and identification of Borrelia burgdorferi sensu lato genospecies in ticks from three different regions in Slovakia. Wiener Klinische Wochenschrift, 119, 534-537. DOI: 10.1007/s00508-007-0851-y 10.1007/s00508-007-0851-ySearch in Google Scholar
Stańczak J., Kubica-Biernat B., Racewicz M., Kruminis-Łozowska W., Kur J. 2000. Detection of three genospecies of Borre lia burgdorferi sensu lato in Ixodes ricinus ticks collected from different regions of Poland. International Journal of Medical Microbiology, 290, 559-56610.1016/S1438-4221(00)80022-3Search in Google Scholar
Sytykiewicz H., Karbowiak G., Werszko J., Czerniewicz P., Sprawka I., Mitrus J. 2012. Molecular screening for Bartonella henselae and Borrelia burgdorferi sensu lato co-existence within Ixodes ricinus populations in central and eastern parts of Poland. Annals of Agricultural and Environmental Medicine, 19, 451-456Search in Google Scholar
Vennestrøm J., Egholm H., Jensen P.M. 2008. Occurrence of multiple infections with different Borrelia burgdorferi genospecies in Danish Ixodes ricinus nymphs. Parasitology International, 57, 32-37 10.1016/j.parint.2007.07.004Search in Google Scholar PubMed
Wodecka B., Leońska A., Skotarczak B. 2010. A comparative analysis of molecular markers for the detection and identification of Borrelia spirochaetes in Ixodes ricinus. Journal of Medical Microbiology, 59, 309-314. DOI: 10.1099/jmm.0.013508-010.1099/jmm.0.013508-0Search in Google Scholar PubMed
Wodecka B., Rymaszewska A., Skotarczak B. 2014. Host and pathogen DNA identification in blood meals of nymphal Ixodes ricinus ticks from forest parks and rural forests of Poland. Experimental and Applied Acarology, 62, 543-555. DOI: 10.1007/s10493-013-9763-x 10.1007/s10493-013-9763-xSearch in Google Scholar PubMed PubMed Central
W. Stefański Institute of Parasitology, PAS
Articles in the same Issue
- Sperm transfer in monogenean (platyhelminth) parasites
- A survey for potentially zoonotic gastrointestinal parasites of dogs and pigs in Cambodia
- Tritrichomonas foetus infection in cat – first detection in Poland
- Association between immunoreactivity to Anisakis spp. antigens and high-risk pregnancy
- Stibarokris mariasi sp. nov. – a new quill mite species (Acariformes: Syringophilidae) parasitizing Puffinus pacificus (Gmelin) (Procellariidae) on Johnston Atoll
- Seroprevalence and correlates of Toxoplasma gondii infection in dairy cattle in northwest China
- Mites and internal parasites associated with the common dung beetle Geotrupes (Anoplotrupes) stercorosus (Hartmann in Scriba, 1791) in Poland
- New species of Cosmocercoides (Nematoda; Cosmocercidae) and other helminths in Gonocephalus liogaster (Squamata; Agamidae) from Peninsular Malaysia
- Cryptosporidium identification in HIV-Infected Humans. Experience from Kinshasa, the Democratic Republic of Congo
- The infection of reintroduced ruminants – Bison bonasus and Alces alces – with Anaplasma phagocytophilum in northern Poland
- Molecular studies on larvae of Pseudoterranova parasite of Trichiurus lepturus Linnaeus, 1758 and Pomatomus saltatrix (Linnaeus, 1766) off Brazilian waters
- Coexistence of Borrelia burgdorferi s.l. genospecies within Ixodes ricinus ticks from central and eastern Poland
- Molecular characterization of cystic echinococcosis: First record of G7 in Egypt and G1 in Yemen
- Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from southern Poland
- A new species of Cosmocerca (Nematoda: Cosmocercidae) and other helminths in Cyrtodactylus gubaot (Squamata: Gekkonidae) from the Philippines
- Alveolar echinococcosis: how knowledgeable are primary care physicians and pharmacists in the Franche-Comté region of France?
- Morphologic and molecular characteristics of Sarcocystis atraii n. sp. (Apicomplexa: Sarcocystidae) infecting the common coot (Fulica atra) from Egypt
- Auto-infection by Echinostoma spp. cercariae in Helisoma anceps
- Risk factors of occurrence of Toxoplasma gondii among horses in the state of Alagoas, Brazil
- Cardiopulmonary helminths in foxes from the Pyrenees
- Risk of soil-transmitted helminth infections on agritourism farms in central and eastern Poland
- Evaluating the Babesia bovis infection of cattle in China with enzyme-linked immunosorbent assay (ELISA)
- Production and preliminary evaluation of Trypanosoma evansi HSP70 for antibody detection in Equids
- Malondialdehyde; Lipid peroxidation plasma biomarker correlated with hepatic fibrosis in human Schistosoma mansoni infection
- A new species of the feather mite genus Tyrannidectes Mironov, 2008 (Acariformes: Proctophyllodidae) from tapaculos (Passeriformes: Rhinocryptidae) in Chile
- Recent study on canine vector-borne zoonoses in southern Slovakia – serologic survey
- Redescription of Paraleptus chiloscyllii Yin et Zhang, 1983 (Nematoda: Physalopteridae) from the Arabian carpetshark Chiloscyllium arabicum (Chondrichthyes: Hemiscylliidae) off Iraq
- A New Species of Ligophorus (Monogenea: Dactylogyridae) from the gills of the Flathead Mullet Mugil cephalus (Teleostei: Mugilidae) from Mexico
- Demodex mites as potential etiological factor in chalazion – a study in Poland
- First report of Schulzia travassosi (Nematoda, Trichostrongylina, Molineoidea) for amphibians of the Chaco region in Argentina and proposal of Oswaldocruzia melanostictusi nov. comb.
- First molecular identification of Ascocotyle (Phagicola) longa in its first intermediate host the mud snail Heleobia australis
- Dog’s genotype of Giardia duodenalis in human: first evidence in Europe
Articles in the same Issue
- Sperm transfer in monogenean (platyhelminth) parasites
- A survey for potentially zoonotic gastrointestinal parasites of dogs and pigs in Cambodia
- Tritrichomonas foetus infection in cat – first detection in Poland
- Association between immunoreactivity to Anisakis spp. antigens and high-risk pregnancy
- Stibarokris mariasi sp. nov. – a new quill mite species (Acariformes: Syringophilidae) parasitizing Puffinus pacificus (Gmelin) (Procellariidae) on Johnston Atoll
- Seroprevalence and correlates of Toxoplasma gondii infection in dairy cattle in northwest China
- Mites and internal parasites associated with the common dung beetle Geotrupes (Anoplotrupes) stercorosus (Hartmann in Scriba, 1791) in Poland
- New species of Cosmocercoides (Nematoda; Cosmocercidae) and other helminths in Gonocephalus liogaster (Squamata; Agamidae) from Peninsular Malaysia
- Cryptosporidium identification in HIV-Infected Humans. Experience from Kinshasa, the Democratic Republic of Congo
- The infection of reintroduced ruminants – Bison bonasus and Alces alces – with Anaplasma phagocytophilum in northern Poland
- Molecular studies on larvae of Pseudoterranova parasite of Trichiurus lepturus Linnaeus, 1758 and Pomatomus saltatrix (Linnaeus, 1766) off Brazilian waters
- Coexistence of Borrelia burgdorferi s.l. genospecies within Ixodes ricinus ticks from central and eastern Poland
- Molecular characterization of cystic echinococcosis: First record of G7 in Egypt and G1 in Yemen
- Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from southern Poland
- A new species of Cosmocerca (Nematoda: Cosmocercidae) and other helminths in Cyrtodactylus gubaot (Squamata: Gekkonidae) from the Philippines
- Alveolar echinococcosis: how knowledgeable are primary care physicians and pharmacists in the Franche-Comté region of France?
- Morphologic and molecular characteristics of Sarcocystis atraii n. sp. (Apicomplexa: Sarcocystidae) infecting the common coot (Fulica atra) from Egypt
- Auto-infection by Echinostoma spp. cercariae in Helisoma anceps
- Risk factors of occurrence of Toxoplasma gondii among horses in the state of Alagoas, Brazil
- Cardiopulmonary helminths in foxes from the Pyrenees
- Risk of soil-transmitted helminth infections on agritourism farms in central and eastern Poland
- Evaluating the Babesia bovis infection of cattle in China with enzyme-linked immunosorbent assay (ELISA)
- Production and preliminary evaluation of Trypanosoma evansi HSP70 for antibody detection in Equids
- Malondialdehyde; Lipid peroxidation plasma biomarker correlated with hepatic fibrosis in human Schistosoma mansoni infection
- A new species of the feather mite genus Tyrannidectes Mironov, 2008 (Acariformes: Proctophyllodidae) from tapaculos (Passeriformes: Rhinocryptidae) in Chile
- Recent study on canine vector-borne zoonoses in southern Slovakia – serologic survey
- Redescription of Paraleptus chiloscyllii Yin et Zhang, 1983 (Nematoda: Physalopteridae) from the Arabian carpetshark Chiloscyllium arabicum (Chondrichthyes: Hemiscylliidae) off Iraq
- A New Species of Ligophorus (Monogenea: Dactylogyridae) from the gills of the Flathead Mullet Mugil cephalus (Teleostei: Mugilidae) from Mexico
- Demodex mites as potential etiological factor in chalazion – a study in Poland
- First report of Schulzia travassosi (Nematoda, Trichostrongylina, Molineoidea) for amphibians of the Chaco region in Argentina and proposal of Oswaldocruzia melanostictusi nov. comb.
- First molecular identification of Ascocotyle (Phagicola) longa in its first intermediate host the mud snail Heleobia australis
- Dog’s genotype of Giardia duodenalis in human: first evidence in Europe
